Vol. 510: 201–213, 2014 MARINE ECOLOGY PROGRESS SERIES Published September 9 doi: 10.3354/meps10790 Mar Ecol Prog Ser

Contribution to the Theme Section ‘ blooms and ecological interactions’ FREEREE ACCESSCCESS Digestion times and predation potentials of noctiluca eating fish larvae and in the NW

Jennifer E. Purcell1,*, Uxue Tilves2, Verónica L. Fuentes2, Giacomo Milisenda3, Alejandro Olariaga2, Ana Sabatés2

1Western Washington University, Shannon Point Marine Center, 1900 Shannon Point Rd, Anacortes, WA 98221, USA 2Institut de Ciències del Mar, CSIC, P. Marítim 37–49, 08003 Barcelona, Spain 3Dipartimento di Scienze e Tecnologie Biologiche ed Ambientali, Università del Salento, 73100 Lecce, Italy

ABSTRACT: Predation is the principal direct cause of mortality of fish eggs and larvae (ichthyo- ). Pelagic cnidarians and ctenophores are consumers of and zooplankton foods of fish, yet few estimates exist of predation effects in situ. Microscopic analyses of the gastric ‘gut’ contents of gelatinous predators reveal the types and amounts of prey eaten and can be used with digestion time (DT) to estimate feeding rates (prey consumed predator−1 time−1). We meas- ured the DT and recognition time (RT) of prey for Pelagia noctiluca, an abundant jellyfish with increasing blooms in the Mediterranean Sea. DT of fish larvae averaged 2.5 to 3.0 h for P. noctiluca (4−110 mm diameter) and was significantly related to jellyfish and larval sizes. In contrast, DT of fish eggs ranged from 1.2 to 44.8 h for jellyfish ≤22 mm diameter (‘ephyrae’), but DT was not sig- nificantly related to ephyra or egg diameter. Approximately half of the eggs ingested were not digested. DT of copepods averaged 4 h. We also measured DT and RT of , euphausiids, and miscellaneous zooplankton. Temperature (20−25°C) generally did not significantly affect DT of any prey. Estimated potential predation effects of ephyrae on fish larvae in the Catalan Sea in 1995 showed great variability among 9 stations (0−3.7% consumed h−1). We discuss how sampling methods contributed to variation in predation estimates and offer recommendations to improve accuracy. Our results enable estimation of predation on ichthyoplankton and competition for zoo- plankton prey, which can have extremely important effects on fish populations globally.

KEY WORDS: Anchovy · Jellyfish · · Fish eggs · Ichthyoplankton · Zooplankton · Competition

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INTRODUCTION nerability to predators (Houde 2008). ‘It is now evi- dent that high and variable predation is the principal, Much of fisheries research has been directed [proximate] agent of mortality’ (Bailey & Houde 1989, towards predicting annual recruitment of fish into Houde 2008, p 63). a fishery. The Critical Period and Aberrant Drift Many species of pelagic cnidarians and cteno- hypotheses (Hjort 1914) inspired 20th-century re - phores eat fish eggs and larvae (ichthyoplankton) cruitment fisheries oceanography research towards (reviewed by Purcell 1985, Purcell & Arai 2001), yet factors affecting the early life history of fish. The studies on the magnitude of this predation remain main factors believed to determine recruitment vari- rare. During the 1980s and 1990s, several studies ability now include the interactions of temperature quantified removal rates of ichthyoplankton by pe - and other physical processes on prey availability and lagic cnidarians and ctenophores in containers rang- larval condition, which in turn determine their vul- ing in size from 25 to 6300 l (reviewed by Purcell &

*Corresponding author: [email protected] © Inter-Research 2014 · www.int-res.com 202 Mar Ecol Prog Ser 510: 201–213, 2014

Arai 2001). The results of those studies were affected ephyrae. We emphasized ichthyoplankton, but also by being conducted in artificial conditions (Purcell & included common zooplankton organisms. Our Arai 2001). A second approach to estimate predation objective was to measure digestion times in order to on ichthyoplankton by pelagic cnidarians and cteno- use this information in combination with gut content phores is to collect the predators in situ, thereby pre- data for P. noctiluca collected at comparable temper- serving their natural prey without experimental in- atures to calculate predator feeding rates and preda- terference. Calculation of ingestion rates (prey eaten tion effects on comparable prey. As an example, we predator−1 time−1) also requires estimation of the time used the gut content data for P. noctiluca ephyrae prey can still be recognized in gut contents; calcula- from Sabatés et al. (2010) to estimate their potential tion of predation effects (% prey standing stock con- predation on fish larvae and copepods off the Cata- sumed time−1) further requires information about the lan coast (NW Mediterranean) in 1995. abundances of the predators and prey in situ. Interest in gelatinous species has resurged re - cently, probably because of their increasing interfer- MATERIALS AND METHODS ence with human enterprises in coastal oceans (Pur- cell et al. 2007). One species of particular concern is Digestion measurements of fish larvae, fish eggs, the holoplanktonic species Pelagia noctiluca that has and zooplankton by Pelagia noctiluca medusae and caused economic damage to aquaculture in northern ephyrae were made in the Catalan Sea during Europe (Doyle et al. 2008, Raffaele 2013) and to cruises on board the RV ‘García del Cid’ (17 June to tourism, fisheries, aquaculture, and energy industries 4 July 2011 and 13 to 21 July 2012). Sea near-surface in the Mediterranean (reviewed by Mariottini et al. temperature and salinity were estimated by the 2008, Canepa et al. 2014). P. noctiluca has a long his- ship’s system. Near-ambient seawater temperature tory of blooms in the Mediterranean Sea (Goy et al. (T in °C) was maintained in the ship’s laboratory by 1989) that appear to be increasing in frequency and means of near-surface water pumped into kreisels duration (Daly Yahia et al. 2010, Kogovšek et al. and water baths containing the experimental con- 2010, Licandro et al. 2010, Bernard et al. 2011). tainers. Fish larvae, fish eggs, and zooplankton used P. noctiluca consumes a variety of prey, including for digestion measurements were selected under copepods and other crustaceans, gelatinous zoo- magnification of a dissecting microscope from plank- plankton, pelagic mollusks, appendicularians, and ton tows of a 60 cm diameter bongo net with 300 µm fish eggs and larvae (Malej 1982, Vu´cti´c 1982, mesh. Fish larvae were identified to the lowest taxon Sabatés et al. 2010, Rosa et al. 2013). Copepods were possible. Anchovy eggs were identified to species by the most numerous prey consumed by ephyrae in their oval shape. Fish larva total length (TL), the NW Mediterranean Sea (Sabatés et al. 2010). cephalothorax length, and fish egg diameter were Although fish larvae averaged <1% of the available measured to the nearest 0.1 mm with calipers with mesozooplankton, they ranged from 5 to 32% of the the aid of a dissecting microscope immediately be - prey in ephyrae; anchovy Engraulis encrasicolus fore they were fed to P. noctiluca. Body lengths of larvae were the most frequently consumed (Sabatés salps (excluding protrusions) and other large species et al. 2010). Thus, P. noctiluca is potentially important were measured to the nearest 0.5 mm. Fish larval as a predator of ichthyoplankton and as a competitor length was converted to dry mass by regressions for of fish larvae and zooplanktivorous fish. Those the most similar taxa in Pepin (1995) and Rossi et al. effects are pervasive but difficult to evaluate. Be - (2006). Our methods, outlined below, were consid- cause predation effects on prey populations increase ered ‘natural feeding’ as defined by FitzGeorge-Bal- with pelagic cnidarian and ctenophore population four et al. (2013) and differed for medusae (observed sizes (Purcell & Arai 2001, Purcell & Decker 2005), visually while in kreisels) and ephyrae (observed ichthyoplankton will likely suffer greater mortality as with a dissecting microscope). populations of these predators increase. P. noctiluca medusae (>22 mm diameter) were col- The in situ feeding rates of P. noctiluca were not lected at night from the surface with a long-handled calculated from gut contents in previous studies due dip net and placed immediately in a bucket with sea- to a lack of data on the digestion times of the various water. They were kept on board in 300 l kreisels with prey types. During cruises of the FishJelly project in weakly flowing seawater, as illustrated by Purcell et 2011 and 2012, we measured digestion length of al. (2013). A prey item held with forceps and touched time and the times prey could be recognized in the to the oral arms was ingested quickly, and the inges- gastric pouches (‘guts’) of P. noctiluca medusae and tion time was recorded. After ingestion, the prey item Purcell et al.: Digestion and predation rates of Pelagia 203

was observed continuously to track its final location in dae) that had been collected during the previous the gastric pouch. Thereafter, each rapidly digesting night using a Bongo net (60 cm diameter, 300 and or transparent prey (i.e. fish larva, salp) was checked 500 µm meshes) from nearby coastal waters. These visually at ≤15 min intervals and each slowly digest- results were compared to the digestion observations ing, conspicuous prey (i.e. euphausiid) at ≤60 min made on board ship. Medusae in which the larvae intervals. Only large fish larvae, euphausiids, and could no longer be seen were also included in the salps were visible once ingested by the medusae; analysis of digestion time. therefore, fish eggs and copepods were not tested on P. noctiluca ephyrae and post-ephyrae with small medusae because they could not been seen after oral arms and (hereafter, all referred to as ingestion. The length of time that prey could still be ‘ephyrae,’ with a diameter ≤22 mm) were collected in seen in the guts was recorded and designated ‘recog- short surface hauls with a Neuston net (1.5 m2 mouth, nition time’ (RT). Prey that could no longer be seen 1 mm mesh). Undamaged ephyrae were kept indi- were considered to be digested, and the time was vidually in 25 to 350 ml glass bowls or beakers in recorded and designated ‘digestion time’ (DT). Eges- which they could swim freely, with container size tion of the prey remains was occasionally observed increasing with specimen size. A fish egg, larva, or (error = 0 min). Otherwise, the error (% of DT) was zooplankter held with forceps and put in contact with calculated from one-half of the final observation inter- each ephyra was ingested quickly. This time of in - val. After digestion of 1 prey item, each medusa was gestion was re corded, and each ephyra was checked fed another prey and the process was repeated. Me - under magnification of a dissecting microscope at dusae appeared to be healthy for 3 to 4 d in the 5 to 60 min intervals, with prey requiring prolonged kreisels and were not used for digestion estimates digestion (fish eggs) being checked at the longer afterwards. The swimming bell diameter then was intervals. DT, RT, and % error were determined as measured to the nearest 1 cm by placing the medusa described for me dusae. Ephyral diameter was meas- subumbrella down on a ruler. ured to the nearest 1 mm with calipers under a dis- Because we could not determine whether fish lar- secting microscope. We used multiple linear regres- vae digested by medusae on the cruise would be rec- sions to test whether DT was related to T, P. noctiluca ognized in gut content analysis, we conducted an diameter, or prey size (largest dimension). Regres- experiment at the Institut de Ciències del Mar in sions were made only when sufficient data were Barcelona, Spain (Table 1). Medusae from laboratory available. When data did not meet assumptions of culture were placed in 300 l kreisels with weakly normality and constant variance, we used log10 flowing ambient seawater and each was given 1 fish transformation before statistical analysis. One-way larva, as above. At 15 to 90 min intervals, 3 to 6 of the ANOVA was used to test for differences in digestion medusae were preserved in 5% formalin solution. times among fish larval taxa and among fish egg Their gastric pouches were examined later with a diameters. Digested and undigested eggs were dissecting microscope to determine whether the prey tested for differences in ephyral sizes and egg sizes could be recognized as a fish larva. This experiment with t-tests. When those data failed to meet assump- was conducted twice (18 and 25 July 2013) with 3 tions after transformation, we used a non-parametric species of larvae: anchovy Engraulis encrasicolus t-test (Mann-Whitney rank sum test). All data were (Engraulidae), round sardinella Sardinella aurita presented as mean ± SD. (Clu pidae), and bullet tuna Auxis rochei (Scombri-

Table 1. Numbers of single fish larvae recognizable in Pelagia noctiluca RESULTS medusae following digestion and preservation at intervals of 15 to 90 min. Re- sults are shown as the number recognizable/number tested. Number of larvae To test when larvae digested by digested = number tested − number recognizable. ‘0’ indicates that all larvae medusae (35.7 ± 2.1 mm diameter) were completely digested. Temperature = 21.3°C. Species were anchovy En- graulis encrasicolus, round sardinella Sardinella aurita, bullet tuna Auxis rochei. could not be recognized as fish larvae NT: not tested with microscopic examination, we examined the gut contents of medu - Species Larval Time interval (min) sae preserved at intervals, as des cri - length (mm) 15 30 45 60 90 bed above (Table 1). All larvae were easily recognizable after 15 and Anchovy & round sardinella 7−9 6/6 6/6 2/11 0/9 NT 30 min. The long, thin anchovy and Bullet tuna 9−11 NT 3/3 3/3 3/3 0/6 round sardinella larvae could not be 204 Mar Ecol Prog Ser 510: 201–213, 2014

re cognized as fish larvae after 45 or 60 min. The with the diameter of P. noctiluca (Fig. 1). Because our larger bullet tuna larvae could still be recognized in methods differed for medusae (>22 mm diameter) the gut contents after 45 or 60 min, but not after 90 min and ephyrae (≤22 mm), we considered the 2 groups of digestion. Based on these results, we removed separately in further analyses. digestion data for 5 anchovy larvae >10 mm long that DTs of both ephyrae and medusae were signifi- could not be seen within swimming medusae on board cantly related to diameter and larval length; DTs ship after 30 min. were shorter for smaller larvae and larger P. nocti - DTs of Pelagia noctiluca medusae and ephyrae fed luca. DTs for fish larvae were not significantly related 1 fish larva averaged 2.5 to 3.0 h (Table 2). DTs of all to T. Similar results were obtained for a multiple re - medusae and ephyrae combined were significantly gression using larval dry mass (DM) instead of related to ephyral diameter (D) and larval length (L), length; however, the relationship with DM (R2 = 2 but not to T (R = 0.258, F3,205 = 24.23, p < 0.001; 0.288, F3,102 = 13.74, p < 0.001, log10 DM t = 3.85; p < log10D t = −8.33; p < 0.001; log10L t = 6.23; p < 0.001; 0.001) was not as strong as with length (Table 2). The T t = 0.66; p = 0.513; log10DT = 0.334 + 0.562 × log10L DTs for ephyrae differed significantly (F5,101 = 346.36, − 0.620 × log10D). DT of combined medusae and p < 0.001) among different types of larvae (Table 3); ephyrae increased with larval length and de creased pairwise comparisons of the DT of anchovy versus all

Table 2. Digestion time (DT) and recognition time (RT) for Pelagia noctiluca given single fish larvae, salps, and copepods un- less noted otherwise. Errors (% of DT) and multiple regression statistics are also given. Salps given to medusae were Salpa fusiformis; those given to ephyrae were Thalia democratica. Data are presented means ± SD, with ranges in parentheses. T: temperature; NS: not significant; NT: not tested

Jellyfish T (°C) Prey length DT (h) Error Regression statistics RT (h) Diameter (D, mm) n (L, mm) (%)

Medusae Fish larvae 48.6 ± 20.6 63 22.7 ± 1.3 14.1 ± 6.5 2.1 ± 2.2 13.3 ± 12.5 R2 = 0.425 0.9 ± 0.8 (25−110) (20.2−25.5) (5−30.0) (0.8−8.3) (0−50) F3,59 = 14.55; p < 0.001 (0.3−5.8) Log10 D t = −0.79; p = 0.432 NS Log10 L t = 6.41; p < 0.001 T t = −1.04; p = 0.300 NS Log10 DT = 0.024 + 1.061 × log10 L Ephyrae Fish larvae 13.4 ± 5.2 107 23.4 ± 0.9 5.9 ± 2.6 3.0 ± 1.7 20.6 ± 25.2 R2 = 0.319 1.2 ± 0.2 (4−22) (20.7−24.4) (1.5−13.0) (0.3−8.3) (0−50) F3,103 = 15.89; p < 0.001 (0.2−5.8) Log10 D t = −2.73; p = 0.007 Log10 L t = 5.71; p < 0.001 T t = −1.37; p = 0.172 NS log10 DT = 1.213 + 0.662 × log10 L − 0.379 × log10 D Medusae Salps 42.2 ± 11.4 30 22.2 ± 1.4 21.3 ± 12.0 2.0 ± 1.8 7.7 ± 9.0 R2 = 0.766 1.8 ± 1.1 (15 − 60) (19.6−23.7) (1.5−40.0) (0.4−6.9) (0−35) F3,103 = 27.23; p < 0.001 (0.2−5.0) D t = 0.66; p = 0.515 NS L t = 4.26; p < 0.001 T t = −2.87; p = 0.008 DT = 12.217 − 0.519 × T + 0.087 × L Ephyrae Salps 10.4 ± 0.6 5 23.4 ± 1.3 5.6 ± 2.6 3.2 ± 2.1 16.2 ± 8.8 NT 1.8 ± 1.4 (10−11) (21.6−25.2) (4.0−10.0) (1.0−5.7) (5−29) (0.4−4.0) Ephyrae 1 copepod 11.8 ± 0.6 51 23.9 ± 0.7 1.3 ± 0.3 4.1 ± 1.3 10.2 ± 5.3 R2 = 0.131 2.2 ± 1.2 (7−22) (22.3−25.0) (1.0−2.0) (1.2−7.8) (0−29) F3,44 = 2.20; p = 0.101 NS (0.7−5.0) D t = −1.66; p = 0.105 NS L t = 1.20; p = 0.235 NS T t = −1.10; p = 0. 276 NS Ephyrae 2−4 copepods 17.0 ± 3.6 4 23 1.1 4.1 ± 0.5 11.4 ± 5.2 NT 1.8 ± 0. 4 (13−20) (3.4−4.7) (7−20) (1.3−2.1) Purcell et al.: Digestion and predation rates of Pelagia 205

Fig. 1. Digestion times of Pelagia noctiluca medusae and ephy rae of fish larvae by type: anchovy Engraulis encrasicolus, thin larvae (sardinellas, gobies), thick larvae (caran gids, sciaenids, serranids, scombrids), and flatfish Aroglossus laterna with re- spect to (a) P. noctiluca diameter, and (b) fish larvae length. Trend lines are best fit linear regressions for all larvae. See Table 2 for multiple regression equations

Table 3. Pelagia noctiluca ephyrae digestion time (DT) and recognition time (RT) of single fish larvae by taxon. Errors (% of DT) are also given. Prey were anchovy Engraulis encrasicolus, serranid Serranus cabrilla, round sardinella Sardinella aurita, mackerel Trachurus mediterraneus, myctophid Ceratoscopelus maderensis, flatfish Aroglossus laterna, and unidentified gobies, sciaenids, and carangids. Data are presented as means ± SD, with ranges in parentheses. T: temperature

Jellyfish T (°C) Fish larvae DT (h) Error (%) RT (h) Diameter (mm) n length (mm)

Ephyrae Anchovy 12.9 ± 5.0 64 23.1 ± 0.9 7.3 ± 2.4 3.5 ± 1.7 13.0 ± 10.2 1.3 ± 0.8 (4−22) (20.7−24.4) (2.5−13.0) (0.8−8.3) (0−50) (0.2−5.8) Serranid 13.2 ± 0.6 6 24.2 ± 0.2 3.8 ± 0.11 2.7 ± 1.5 17.8 ± 6.9 1.8 ± 0.3 (9−13) (23.7−24.4) (3.5−4.0) (1.3−2.6) (0−24) (1.4−2.2) Round sardinella 13.3 ± 4.2 7 23.7 ± 0.2 6.0 ± 1.4 1.7 ± 0.8 10.8 ± 7.9 0.8 ± 0.4 (10−22) (23.3−24.4) (4.0−8.0) (1.0−2.8) (9−24) (0.4−1.5) Goby 9.8 ± 2.8 6 24.1 ± 0.5 2.2 ± 0.9 1.2 ± 0.9 35.0 ± 18.2 0.6 ± 0.3 (8−15) (23.5−24.4) (1.5−4.0) (0.5−2.7) (6−50) (0.3−1.1) Scombrid, sciaenid, carangid 13.5 ± 5.5 24 23.9 ± 0.8 3.6 ± 1.5 2.2 ± 1.2 22.0 ± 17.9 1.2 ± 0.6 (7−22) (21.1−24.4) (1.5−7.0) (0.3−5.1) (0−50) (0.4−2.5) Flatfish 17.3 ± 5.8 6 23.8 ± 0.7 3.5 ± 0.6 2.8 ± 2.2 14.9 ± 19.0 1.3 ± 1.2 (10−22) (23.0−24.4) (3.0−4.0) (0.9−5.6) (0−50) (0.2−3.2) other types of larvae were significantly different (RTs) were approximately half of the DTs for both (Holm-Sidak method, t = 18.12 to 29.63, p < 0.001), medusae and ephyrae. and DTs of goby larvae also differed significantly Fish eggs were digested more slowly (1.2−44.8 h) from DTs of serranid and flatfish larvae (t = 3.08 and than fish larvae by P. noctiluca ephyrae (Table 4, 2.80, respectively, p < 0.01). Thus, long, thin larvae Fig. 2). About half of all eggs tested (29 of 56) were (anchovies, sardinellas, gobies) were digested more egested undigested after many hours, but interest- rapidly than short, thick larvae (scombrids, caran - ingly, all anchovy eggs were digested. The sizes of gids, serranids, flatfish; Fig. 1). The lengths of time ephyrae that had not digested eggs did not differ that they were recognizable as fish larvae in the guts from those that had (t-test, t51 = 1.445, p = 0.155); 206 Mar Ecol Prog Ser 510: 201–213, 2014

Table 4. Pelagia noctiluca ephyrae digestion time (DT) and recognition time (RT) of single fish eggs by diameter. Eggs 0.8 mm in diameter are presented in 2 groups (anchovy and those other than anchovy). Retention times are for undigested eggs that were egested. Errors (% of DT) are also given. Temperatures were 23.4 ± 0.5°C (22.3−25.2°C). Data are presented as means ± SD, with ranges in parentheses. Percentages of each egg size digested are in square brackets. Errors reflect digested and undigested eggs; NA: not applicable

Fish egg Digested eggs Undigested eggs diameter Ephyra n DT (h) RT (h) Error (%) Ephyra n Retention (mm) (mm) (mm) (h)

0.6 [75%] 9.9 ± 3.1 9 8.2 ± 2.2 6.1 ± 2.1 15.8 ± 2.2 8.7 ± 1.5 3 12.1 ± 6.3 (7−15) (4.3−10.6) (3.2−9.5) (13−20) (7−10) (5.2−17.5) 0.8 [45.2%] 12.1 ± 4.3 14 17.4 ± 12.0 14.8 ± 13.0 19.0 ± 18.8 9.8 ± 3.7 17 12.6 ± 7.9 (8−22) (3.8−44.8) (2.3−43.0) (6−50) (5−20) (2.8−29.2) 0.8 anchovy [100%] 9.7 ± 0.5 6 8.5 ± 5.4 6.3 ± 3.1 19.8 ± 6.2 NA 0 NA (9−10) (1.2−17.8) (4.5−12.5) (15−30) 1.0 [0%] 8.0 ± 1.0 0 NA NA NA 8.0 ± 1.4 2 22.7 ± 1.0 (7−9) (7−9) (22.0−23.4) 1.1 [0%] 13.3 ± 6.5 0 NA NA NA 15.0 ± 5.1 6 3.0 ± 0.9 (7−20) (10−22) (1.8−4.2)

Fig. 2. (a) Pelagia noctiluca ephyral digestion and retention times of fish eggs with respect to egg diameter. Time (h) that eggs were inside ephyrae. (b) Size of ephyrae compared to size of digested and undigested eggs. In (b), ephyral diameters for di- gested eggs were offset by +0.3 mm and only 1 point is shown for anchovy (of 6 at 9−10 mm) to enable them to be better seen thus, small ephyral size did not explain why some undigested eggs were significantly related to ephyral eggs were not digested. Similarly, egg sizes did not size, T, or egg size (F3,28 = 1.071, p = 0.377 and F3,22 = differ between those digested or undigested (Mann- 0.622, p = 0.608, respectively). RT of digested fish Whitney U = 296.50, p = 0.194) although no 1.0 or eggs were 75−85% of the DT for ephyrae, and RT of 1.1 mm eggs were digested. To test whether eggs undigested eggs were 100% of retention times. would be digested without the chorion, it was dis- DT and RT of copepods could only be measured for sected from 4 of the 1 mm eggs, which otherwise ephyrae (Table 2). DTs of single copepods by were not digested by ephyrae. These embryos were ephyrae averaged 4 h and were not significantly digested rapidly by the ephyrae (1.78 ± 0.46 h; related to prey or ephyral size, or T. We gave 2 to 4 Fig. 2), suggesting that the chorion protected the copepods only to 4 ephyrae, but average digestion eggs from digestion. DTs of eggs differed signifi- time remained ~4 h. RTs of copepods were about half cantly by diameter (F3,29 = 5.68, p = 0.003), with of the DTs for ephyrae. 0.8 mm eggs requiring longer to digest than all Salps were very abundant and were eaten by me- others. One 3 mm diameter egg was digested in dusae in 2011 (J. E. Purcell pers. obs.). DTs of large 22.4 h by a 22 mm ephyra. Neither DTs nor RTs of salps Salpa fu si formis by medusae averaged 2 h and Purcell et al.: Digestion and predation rates of Pelagia 207

were sig ni fi cantly related to salp length and tempera- DT of anchovy eggs by quinquecirrha ture (Table 2). The few salps Thalia democratica medusae (3.7−5.2 h, mean 4 h) and Stomolophus small enough to be ingested by ephyrae were meleagris (3 h) were within the range for P. noctiluca digested in ~3 h. ephyrae (1.2−17 h, mean 8.5 h), but shorter on aver- P. noctiluca eats a variety of zooplankton, but di - age. DTs of ~1 mm copepods by P. noctiluca ephyrae gestion times previously were unavailable. DTs of were similar to those of other species of comparable euphausiids (n = 10, 10−20 mm TL) by medusae aver- sizes even at temperatures that were 10°C lower aged 5.0 ± 2.4 h. Velella velella colonies were eaten (Table 5). Our results are also comparable to other by medusae in situ (V. L. Fuentes et al. pers. obs.). species digesting cladocerans and appendicularians. DTs of 15 and 26 mm long colonies by 2 medusae The cladoceran Evadne sp. was digested by Aurelia were ~3.7 h, and those of 1 to 3 mm long colonies by aurita ephyrae in 3.4 h at 4−5°C (Sullivan et al. 1997). 4 ephyrae were ~5.3 h. The chitin sail of V. velella Digestion of appendicularians was very rapid by was still recognizable after egestion. The necto - hydromedusae (<2 h; Larson 1987b) and by S. melea- phores of 2 polygastric colonies of the siphonophore gris at 28−30°C (1.5 h; Larson 1991). We are unaware Muggiaea atlantica were egested with their firm of other DTs for gelatinous predators of salps, mesoglea intact from medusae after 5.0 and 6.5 h. pteropods, or stages of euphausiids other than eggs Cladocerans (Penilia sp. and Podon sp.) were diges - or nauplii (see Martinussen & Båmstedt 2001). ted by ephyrae in 3.0 ± 1.7 h (n = 17). DTs of euphau- Our estimates of DT and RT in P. noctiluca were siid furcilia larvae (n = 13, 3−11 mm TL) for ephyrae constrained by the numbers and sizes of medusae averaged 5.0 ± 0.9 h. DTs by ephyrae were short for available and the relatively narrow range of ambient 2 appendicularians (<1 h) and 1 chaetognath (1−2 h). seawater temperature. Too few medusae were pres- Coiled pteropods (n = 3, 0.5 mm), whose shells were ent to allow repeated microscopic analysis to follow recognizable until egestion, were digested in ~4 h by digestion over time, which could have damaged the ephyrae. RTs of the crustaceans were 45 to 65% of specimens, or to preserve them for gut analysis to DTs. RTs of shelled pteropods and the cnidarians confirm complete digestion or recognition. P. nocti - were 100% of DT. luca inhabits a wide range of temperatures from deep waters at <14°C to the surface at >26°C in the Mediterranean Sea. Therefore, DT and RT should be DISCUSSION measured over that range of temperatures, which large medusae traverse on daily vertical migrations. Digestion and recognition times Because we followed prey items in swimming me - dusae, 2 problems resulted. First, the end-point of Gut contents of gelatinous predators in combina- digestion was usually very subjective. Second, we tion with DT can be used to determine in situ preda- were unable to measure digestion of small prey tion rates (prey consumed predator−1 time−1), and in (copepods, most fish larvae, and fish eggs) by combination with population densities of the preda- medusae; therefore, additional experiments need to tors and prey, they can be used to estimate predation be conducted in which digestion of prey can be mon- effects (% prey consumed time−1). Even though Pela- itored more precisely. Our study was also limited by gia noctiluca blooms in tropical to temperate oceans monitoring digestion of single prey items. Because of around the world (Kramp 1961), few studies exist on their small size, ephyrae may not catch several prey DT. Gordoa et al. (2013) mentioned 18 ± 5 h as the DT items concurrently (but see Fig. 3); however, me - of bluefin tuna Thunnus thynnus eggs by ‘burst feed- dusae usually contain numerous prey (J. E. Purcell & ing’ P. noctiluca ephyrae. We also only know the DT U. Tilves pers. obs.), which affected DT measured for for P. noctiluca medusae consuming lei- small A. aurita (Martinussen & Båmstedt 2001, Fitz- dyi ctenophores (Tilves et al. 2012). George-Balfour et al. 2013). Martinussen & Båmstedt (2001) comprehensively The lack of digestion of about 50% of the fish eggs summarized earlier studies on DTs of fish larvae, fish by ephyrae raised interesting questions. Although eggs, and zooplankton by gelatinous predators. The small ephyral size did not explain that phenomenon DTs of fish larvae in our study were similar to those in (Fig. 2b), we could not measure digestion of fish eggs other studies that included larvae and medusae of by medusae because we could not visually follow comparable sizes, even when the temperatures were such small prey inside them. As ephyrae grew, the 10°C lower (Table 5). Few DTs were available for fish number and length of the digestive filaments in the eggs, and no other studies used ephyrae and eggs. gastric pouches increased (J. E. Purcell pers. obs.). 208 Mar Ecol Prog Ser 510: 201–213, 2014

Table 5. Selected studies reporting digestion times (DT) for medusae and ctenophores eating fish larvae or eggs and copepods. The percentages of the standing stocks consumed and percentages of prey in the gut contents also reported if available. If more than 1 prey item was digested, the numbers are given in parentheses. T: temperature; NG: not given; lg: large; sm: small; n: number

Predator species Prey T DT Notes Standing stock eaten Reference Diameter n Type (n) Size (°C) (h) (% d−1) (% of (mm) (mm) prey)

Fish larvae Aequorea victoria Clupea haren- 9−14 8−12 1.6−5.2 DT increased with 0.8−73 0−97 Purcell (1989), 49−68 204 gus pallasi prey size and number, Purcell & Arai larvae (1−15) decreased with T (2001) Aurelia aurita C. harengus 11 9.5 3.9 ± 0.5 NG NG Martinussen & 20−75 10 larvae Båmstedt (1999) A. aurita Pleuronectes NG 7 2.3 ± 1.0 ~1a,c <2a,c Sullivan et al. 3−25a 40a americanus larvae (1994) Chrysaora Anchoa mitchilli 3 26 1.1 ± 0.5 29 ± 14 0−8.8 Purcell et al. quinquecirrha larvae (1−9) (1994) NG 7 Pelagia noctiluca Engraulis en- 1.5−30 20−25 0.7−8.3 DT decreased with 1.2−13.4 0−13.6 This study; 4−110 175 crasicolus & jelly size, increased Sabatés et al. other larvae with larval size (2010) Fish eggs Cyanea capillata Fish eggs NG NG 5.3 0.1–3.8 14.3 Fancett (1988), ~2−100 ~35 20−25b Fancett & Jenkins (1988) Pseudorhiza Fish eggs NG NG 3.3 0.1–2.4 40.8 Fancett (1988), haeckeli 20−25b Fancett & ~5−100 ~35 Jenkins (1988) Stomolophus Fish eggs 0.6−0.8 28−30 3 NG <1 Larson (1991) meleagris 15−100 165 C. quinquecirrha A. mitchilli eggs ~1.0 26 3.7−5.2 DT independent of 14 ± 4 0.1−90 Purcell et al. 23−44 16 (9−52) 3.9 ± 0.8 egg numbers and (1994) medusa size P. noctiluca E. encrasicolus 0.6−3 23−25 1.2−44.8 DT independent of NG NG This study 7−22 29 & unident. eggs ephyra and egg sizes and T Mnemiopsis leidyi A. mitchilli eggs ~1.0 24 DT 0−36 NG Purcell et al. lg 50−75 20 (1−2) lg 0.6 ± 0.1 9 ± 14 NG (1994) sm 7−22 13 sm 1.0 ± 0.4 Copepods C. capillata Copepods NG NG 1.7 DT 0.1–1.6d 10.7 Fancett (1988), ~2−100 ~35 20−25b Fancett & Jenkins (1988) P. haeckeli Copepods NG NG 1.7 DT 0.2–4.8d 32.8 Fancett (1988), ~5−100 ~35 20−25b Fancett & Jenkins (1988) S. meleagris Calanoids 0.3−1.5 28−30 1.5 DT NG 4.3 Larson (1991) 15−100 165 A. aurita Pseudocalanus 1.4 9.5 3.7 ± 1.7 DT NG NG Martinussen & 4.5−13.5 24 elongatus Båmstedt (1999) A. aurita Temora 1 9.5 3.2 ± 0.9 DT NG NG Martinussen & 8.7−13 6 longicornis Båmstedt (1999) A. aurita Calanus 2.3 9.5 1.5−7.7 DT decreased with NG NG Martinussen & 4.3−54 39 finmarchicus 5.2 ± 2.0 medusa size Båmstedt (1999) A. aurita Acartia NG 7 2.3±1.0 DT <25a,c 0−70 Sullivan et al. 3−25 mma 40a hudsonica (1994) C. quinquecirrha Acartia tonsa 1 20−27 1.1−6.2 DT decreased with T 1−94 55−71 Purcell (1992) 25−126 16 (3−631) 3.5 ± 1.1 P. noctiluca Calanoids 1−2 22.3−25 1.2−7.8 DT independent of <0.1−3 43−86 This study 7−22 53 4.1 ± 1.3 ephyral and prey size and T M. mccradyi = leidyi Acartia tonsa 1 25−27 1 DT 12−82c 13c Larson (1988) NG 39 34 ± 28c aIn mesocosm; bestimated from Port Phillip Bay summer water temperature; ccalculated from data in paper; dlaboratory feeding estimates Purcell et al.: Digestion and predation rates of Pelagia 209

sect perpendicular to the coast at 3 stations (Shelf: over the shelf; Front: over the slope at a shelf-break front; Open Sea: in the open sea) during 18 to 23 June 1995. Sampling was repeated 3 times at each station, and temperature was measured at each station with a CTD. Zooplankton, jellyfish, and fish larvae were sampled by oblique tows of a 60 cm diameter bongo net with a flowmeter and 500 m mesh from near- bottom (70−80 m) to the surface over the shelf or from 200 m to the surface at the front and in the open sea (≥1000 m depth). The duration of the tows ranged from 6 min at shallow shelf stations to 23 min at the front and open sea stations. Net samples were fixed in a 5% formaldehyde–seawater solution. P. noctiluca ephyrae (≤12 mm diameter), and fish larvae were Fig. 3. Pelagia noctiluca ephyra collected from the surface at counted and identified to the lowest possible taxo- night and immediately preserved on 4 July 2011. The ephyra contained 2 anchovy larvae (~10 mm long) and 1 nomic level from whole preserved samples aided by a unidentified fish egg (0.9 mm diameter; indicated by arrow). dissecting micro scope. All copepods were counted Ephyra preserved diameter is 7 mm from 1/256 to 1/32 aliquots obtained with a plankton splitter. The gut contents of all ephyrae in the samples The ephyrae collected by Sabatés et al. (2010) did were identified, counted, and measured; only partly not contain any fish eggs, although they were avail- digested prey were included to ensure that the prey able for consumption (A. Sabatés pers. obs.). There- items had not been captured while in the net. fore, we do not know whether P. noctiluca medusae Although Sabatés et al. (2010) presented average >22 mm would digest all fish eggs. predation by location (Shelf, Front, Open Sea), we On the other hand, the fish eggs may be resistant to calculated feeding at each of the 3 stations per loca- digestion. Baltic cod Gadus morhua callariasadus tion. Individual feeding rates of P. noctiluca ephyrae eggs were rejected by M. leidyi ctenophores; cteno- on fish larvae and copepods were calculated from the phores that had ingested eggs subsequently ejected numbers of each prey type in the gut contents at each 12 of 14 eggs undigested after 2 h at 22°C and 3 d at station divided by the DT of 107 fish larvae or 53 7°C (Jaspers et al. 2011). Plaice Pleuronectes platessa copepods at the mean surface water temperature in eggs similarly were ingested, but were egested undi- 1995 (20.4°C), as calculated from mean prey sizes gested ‘after some hours’ by Bolinopsis infundibulum and regression equations in Table 2. Individual feed- ctenophores (Gamble 1977). Most (98−99%) bivalve ing rates were multiplied by ephyral densities and veligers were not digested or killed by C. quinquecir- divided by prey densities at each station to estimate rha medusae (Purcell et al. 1991). ‘Passing alive’ of the effects of the ephyrae on the prey populations pelagic larvae of benthic invertebrates through their (% prey standing stock consumed h−1). To estimate predators has been described previously (Milei- the potential daily predation at each location, we kovsky 1974), but we could find no further informa- assumed that feeding and digestion were continuous tion about fish eggs. Unfortunately, we were unable over the 8 h periods represented by the samples at to determine whether the eggs had been killed by each location (day, dawn/dusk, night) and multiplied the ephyrae or remained viable. the hourly rates by 8 and then summed the 3 stations. Estimates of potential predation by ephyrae on fish larvae were highly variable among the 9 stations Potential predation effects by Pelagia noctiluca (Fig. 4). Ephyrae were much more abundant (13.4 m−3) on fish larvae and copepods at the Front at night (01:00 h) than at other stations (<1 m−3). The incidences of feeding (ephyrae with The DT and RT of P. noctiluca are valuable instru- prey) at the Front were only 6 to 13%, probably ments for estimating predation on prey populations in reflecting damage to the ephyrae and loss of prey in situ. We, therefore, chose a study conducted in the the 200 m depth tows. Fish larvae were of average Catalan Sea (Sabatés et al. 2010) to illustrate this abundance at that station, and the highest levels of method and problems we encountered. In the Sabatés predation (3.7% of the larvae h−1) occurred there at et al. (2010) study, sampling was conducted on a tran- night (Fig. 4). Although ephyrae were found at low 210 Mar Ecol Prog Ser 510: 201–213, 2014

Table 6. Estimated potential predation effects (% prey con- sumed d−1) of Pelagia noctiluca ephyrae on fish larvae and copepods in the northwest Mediterranean Sea in June 1995

Prey type Location Prey in Ephyrae Prey guts examined consumed (n) (n) (% d−1)

Fish larvae Shelf 2 145 3.6 Front 26 4400 13.4 Open sea 5 1135 1.2 Copepods Shelf 18 145 0.42 Front 110 4400 0.31 Open sea 48 1135 0.31

the ephyrae only at night (22:00 h) on the Shelf, when we estimated that 1.2% h−1 could have been con- sumed. In the Open Sea, ephyral densities, feeding incidences (9−10% in 200 m tows), and predation effects were low (0−0.7% h−1; Fig. 4). Daily potential predation effects on fish larvae at each location ranged from 1.2 to 13.4% d−1; Table 6). Estimated potential predation effects by P. noctiluca ephyrae on copepods were much lower than on fish larvae (Fig. 4). Although copepods were very abun- dant at the Front station at night, the estimated potential predation effect was low (0.05% h−1) because of the low feeding incidence. The highest predation effect (0.11% h−1) was at night on the shelf, again probably because of the high feeding incidence (25%). The daily potential predation effects on cope- pods at each station ranged from 0.30 to 0.42% d−1; Table 6). The predation effects of ephyrae on cope- pods were much lower (≤0.42% d−1) than on fish lar- vae (≤13.4% d−1) due to the 50- to 500-fold greater densities of copepods. Even though the sampling methods of Sabatés et al. (2010) were standard for fisheries oceanography, they illustrated some problems for estimating preda- tion effects on fish larvae by P. noctiluca. First, we believe that the net sampling damaged the ephyrae and reduced their apparent feeding. That was indi- cated by the higher feeding incidence on the shallow Fig. 4. Abundances and predation effects of Pelagia nocti - shelf where tows were half as deep as at the other luca ephyrae on fish larvae and copepods according to sta- tion (stn) and time of day in the northwestern Mediterranean stations. This likelihood also was clearly illustrated Sea during 18 to 23 June 1995. Three stations each were by the gut contents of ephyrae dipped from the sur- over the shelf, at a shelf-break front, or in the open sea along face in 2011 to 2012 (Fig. 3), which contained fish a transect perpendicular to the coast. (a) Ephyrae densities, eggs and more fish larvae than in 1995. Additionally, (b) fish larvae densities, (c) predation effects on fish larvae, (d) copepod densities, and (d) predation effects on copepods the 60 cm diameter net was too small to adequately sample the larger medusae. Thus, feeding by P. noc- densities on the Shelf (0−0.03 m−3), fish larval densi- tiluca was underestimated with these net samples. ties were highest there (0.8−1.2 m−3), and feeding Other biases in the predation estimates resulted be- incidences were high (14−33%) where tows were cause the oblique tows of Sabatés et al. (2010) ob- from only 70 to 80 m depth. Fish larvae were found in scured the patterns of P. noc- Purcell et al.: Digestion and predation rates of Pelagia 211

tiluca and their prey. The medusae are known to mi- could be important predators of fish eggs and larvae. grate near to the surface at night (Ferraris et al. 2012), Larson (1987a) stated that fish eggs were the most nu- and the ephyrae move near the surface during the merous prey items in 50 medusae, with as many as 10 night (Gordoa et al. 2013; V. L. Fuentes et al. pers. obs.). eggs medusa−1. Sabatés et al. (2010) found that fish lar- Anchovy larvae also migrate towards the surface at vae represented ~12% of the prey items in ephyral gut night (Sabatés et al. 2008). Thus, the oblique net tows contents in the spring. Fish larvae and eggs re- in 1995 did not reflect the fine-scale patterns of over- presented 0.2 and 1.1%, respectively, of the prey in lap of ephyrae and larvae over 24 h, which were not medusae collected throughout a year (Rosa et al. 2013). known, but may have extended the duration of over- Gelatinous predators have been demonstrated to re- lap. The variable sampling times at the different sta- duce populations of fish larvae (Purcell & Grover 1990). tions in 1995 also made predation estimates difficult to Gelatinous predators consume a variety of fish compare. If we had used RT instead of DT to calculate species in the plankton, including commercially va lu- predation effects, the effects would have been ap- able species. The siphonophore Rhizophysa eysen - proximately doubled. We consider the predation esti- hardti consumed fish larvae in 5 families (Purcell mates presented here to be rough approximations. 1981). The scyphomedusae Cyanea capillata and Thus, our recommendations for use of the gut- Pseu do rhiza haeckeli consumed 4 kinds of larvae and content method to estimate gelatinous predator con- eggs (Fancett 1988). S. meleagris con sumed 4 kinds sumption of ichthyoplankton and mesozooplankton of eggs (Larson 1991). Similarly, the large hydrome- are as follows: dusan Aequorea victoria consumed larvae of at least • Collect specimens for gut contents individually, 10 species of fishes and eggs of at least 3 species (Pur- not in plankton nets, and preserve them immediately. cell 1989). Eight species of larvae were eaten by • Collect gut-content specimens from all appropri- P. noctiluca ephyrae (Sabatés et al. 2010). Additional ate depths, not only at the surface. studies conducted since the reviews by Purcell (1985) • Appropriate sampling methods should be chosen and Purcell & Arai (2001) have shown that the cubo- with consideration of the depth distribution patterns medusae Chironex fleckeri, Tamoya hap lo nema, and of predator and prey species during day and night. Chiropsalmus quadruma nus eat fish (Carrette et al. • Use ambient temperature to measure digestion 2002, Nogueira Júnior & Haddad 2008). Young fish and recognition times. and fish eggs represented 5.2 and 1.2%, respectively, • Different digestion methods may be best depend- of the prey items in the pleustonic hydrozoan Velella ing on predator and prey characteristics (e.g. Purcell velella (Purcell et al. 2012). Thus, the potential effects et al. 1991, FitzGeorge-Balfour et al. 2013). of gelatinous pre dators on fish are great. • The duration between ingestion and when prey Mesozooplankters are the main components of the can still be recognized in microscopic gut-content diets of many fish and pelagic cnidarians and cteno - analysis (RT) is the most appropriate measure for use phores, and dietary overlaps have been shown (Pur- in feeding estimates using gut contents. cell & Grover 1990, Purcell & Sturdevant 2001, Bro- • Use data for ephyral size and ichthyoplankton deur et al. 2008). The small percentages of the species and size consumed for greatest accuracy. cope pod standing stocks consumed by P. noctiluca • Determine densities, depths, and size distribu- ephyrae may seem unimportant, but the combined tions of the gelatinous species and their prey to esti- predation of the suite of gelatinous predators (Fuen - mate predation effects (% prey standing stock con- tes et al. 2010, Sabatés et al. 2010, Canepa et al. 2014) sumed d−1). removes food that otherwise could be consumed by fish. Studies of in situ predation by gelatinous species eating mesozooplankton are more numerous than Effects of gelatinous zooplankton as predators studies on ichthyoplankton (e.g. Larson 1987b, 1988, and competitors of fish Purcell 1997, 2009). Predation effects on mesozoo- plankton, primarily copepods, vary greatly depend- Surprisingly few studies have addressed consump- ing on the abundance of the predators (summarized tion of fish eggs and larvae by gelatinous predators in by Purcell & Arai 2001). Competition for prey re- situ. Whenever such studies were conducted, the pre- quires that prey are limiting, and when abundant, dation effects were substantial (reviewed by Purcell pelagic cnidarians and ctenophores can reduce cope- 1985, Purcell & Arai 2001). Ichthyoplankton often con- pod populations (e.g. Purcell & Decker 2005). stitutes large proportions of prey found in the gut con- We believe that existing evidence of gelatinous tents (Table 5). P. noctiluca ephyrae and medusae species as important predators of ichthyoplankton 212 Mar Ecol Prog Ser 510: 201–213, 2014

and mesozooplankton covers only a small fraction of Carrette T, Alderslade P, Seymour J (2002) Nematocyst and the extent of their predation. Past studies have con- prey in two Australian cubomedusans, Chironex fleckeri and Chiropsalmus sp. Toxicon 40:1547−1551 sidered only a few of the >1400 species of gelatinous Condon RH, Duarte CM, Pitt KA, Robinson KL and others predators that inhabit all depths of estuaries and (2013) Recurrent jellyfish blooms are a consequence of oceans (Purcell et al. 2007). The studies were con- global oscillations. Proc Natl Acad Sci USA 110: 1000–1005 ducted only in near-surface waters, whereas concen- Daly Yahia MN, Batistic M, Lu i D, Fernández de Puelles ML and others (2010) Are outbreaks of Pelagia noctiluca trations of ichthyoplankton, mesozooplankton, and (Forskål, 1771) more frequent in the Mediterranean predators often occur at sub-surface hydrographic basin? ICES Coop Rep 300: 8−14 discontinuities (clines) (Graham et al. 2001, Purcell et Doyle TK, De Haas H, Cotton D, Dorschel B and others al. 2014). The studies have also been limited spatially (2008) Widespread occurrence of the jellyfish Pelagia and temporally. Although P. noctiluca has been stud- noctiluca in Irish coastal and shelf waters. J Plankton Res 30: 963−968 ied in only a few locations, primarily in Irish waters Fancett MS (1988) Diet and prey selectivity of scyphomedu - (Doyle et al. 2008, Bastian et al. 2011) and the Medi- sae from Port Phillip Bay, Australia. Mar Biol 98: 503−509 terranean Sea, this species is found in tropical to tem- Fancett MS, Jenkins GP (1988) Predatory impact of scypho - perate oceans around the world (Kramp 1961). Stud- medusae on ichthyoplankton and other zooplankton in Port Phillip Bay. 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Submitted: November 18, 2013; Accepted: March 17, 2014 Proofs received from author(s): May 9, 2014